Gustatory neural coding in the amygdala of the alert macaque monkey

Abstract

1. Neurons in the amygdala are implicated in mediating hedonic appreciation, emotional expression, and conditioning, particularly as these relate to feeding. The amygdala receives projections from the primary taste cortex in monkeys, offering a route by which it could gain access to the gustatory information required to guide feeding behavior. We recorded the activity of 35 neurons in the amygdala of alert rhesus macaques in response to a range of gustatory intensities and qualities to characterize taste-evoked activity in this area. 2. The stimulus array comprised 26 chemicals, including four concentrations of each of the four basic taste stimuli, a series of other sugars, salts, and acids, monosodium glutamate, and orange juice. 3. Neurons responsive to taste stimulation could be found in a 76-mm3 region of the amygdala, centered 9.1 mm lateral to the midline, 14.9 mm anterior to the interaural line, and 25.7 mm below the surface of the dura. They composed 7.2% (35/484) of the cells tested for gustatory sensitivity in the amygdala. 4. The mean spontaneous activity of taste cells was 8.2 +/- 2.3 (SE) spikes per second. This rather high level provided an opportunity for reductions from spontaneous rate that was used regularly in the amygdala. When these negative response rates were included, the mean breadth-of-tuning coefficient of this sample of taste cells was 0.82. There was no strong evidence for gustatory neuron types, nor were functionally similar cells located together in a chemotopic arrangement. 5. Responses across 1.5 log units of stimulus concentration were nearly flat, with increasing excitation in some neurons largely offset by increasing inhibition in others. Taking the absolute value of the evoked activity, concentration-response functions rose monotonically to all basic stimuli except HCl, but were not sufficiently steep to account for human psychophysical data. The neural response to HCl did not rise with stimulus concentration within the range used. 6. Neural patterns representing the taste qualities of the basic stimuli were less sharply separated in the amygdala than at lower-order gustatory relays. Glucose elicited activity patterns that were most distinct from those of the nonsweet chemicals; those associated with NaCl were next most distinct. There was no clear separation between the patterns generated by chemicals that humans describe as sour and bitter. Monosodium glutamate evoked responses that did not correlate well with those of any basic stimulus, implying that its quality cannot be subsumed under the four basic tastes.(ABSTRACT TRUNCATED AT 400 WORDS)

A Role for the Right Anterior Temporal Lobe in Taste Quality Recognition

“…These results suggest that hedonic assessment may contribute to discrimination of taste quality; however, it is unlikely that hedonic processing is performed within the PGA, because lesions in this area do not disturb preference-aversion learning (for review, see Rolls, 1993). Cells that respond to taste stimulation have been identified in the amygdala of the macaque monkey with use of single-cell recording techniques (Scott et al, 1993). Such neurons show no evidence of chemotopic arrangement, and they respond less selectively to the basic taste qualities than do neurons located at lower-order gustatory relays (Scott et al, 1993).…”

“…Cells that respond to taste stimulation have been identified in the amygdala of the macaque monkey with use of single-cell recording techniques (Scott et al, 1993). Such neurons show no evidence of chemotopic arrangement, and they respond less selectively to the basic taste qualities than do neurons located at lower-order gustatory relays (Scott et al, 1993). Furthermore, responses across 1.5 log units of stimulus concentration are nearly flat.…”

“…Furthermore, responses across 1.5 log units of stimulus concentration are nearly flat. Scott et al (1993) have suggested therefore that taste-related activity in the amygdala does not provide an adequate basis for the discriminative capacity of humans or monkeys with regard to either stimulus quality or concentration. Rather, these authors suggest that the amygdala contributes to gustatory processes by "imparting hedonic appreciation and emotional significance to taste experience," as the amygdala has long been implicated in hedonic processing (Jones and Mishkin, 1972;Ono et al, 1983;LeDoux, 1987).…”

Pleasurable behaviors reduce stress via brain reward pathways

“…Because the hedonic/rewarding properties of sucrose, saccharin, or sex appear sufficient to dampen subsequent stress responses, we hypothesized that brain reward regions, such as the BLA, are likely to mediate these effects. Neuronal activity in the amygdala, including the BLA, is altered in humans and other animals while they are engaging in pleasurable behaviors, including eating ap- petizing foods (20)(21)(22)(23). The amygdala is also activated in humans and other animals during stress (24,25), and the BLA subregion is implicated in neuroendocrine and behavioral stress responses (26)(27)(28).…”

Consumer Evaluation of Low Sodium Mozzarella Cheese and Development of a Novel Method for Evaluating Emotions

“…In addition to the importance of the OFC, the amygdala is involved in feeding control due to its sensitivity to taste inputs and responses from other brain regions including the primary taste cortex which sends gustatory information to nuclei in three regions of the amygdala (Scott et al, 1993). The amygdala has been found to be specifically important for sodium intake, with lesions to the central amygdala causing decreased sodium intake (Li et al, 2012).…”